Abstract
The metal-reducing bacterium Geobacter sulfurreducens requires the expression of conductive pili to reduce iron oxides and to wire electroactive biofilms, but the role of pilus retraction in these functions has remained elusive. Here we show that of the four PilT proteins encoded in the genome of G. sulfurreducens, PilT3 powered pilus retraction in planktonic cells of a PilT-deficient strain of P. aeruginosa and restored the dense mutant biofilms to wild-type levels. Furthermore, PilT3 and PilT4 rescued the twitching motility defect of the PilT-deficient mutant. However, PilT4 was the only paralog whose inactivation in G. sulfurreducens lead to phenotypes associated with the hyperpiliation of non-retractile mutants such as enhanced adhesion and biofilm-forming abilities. In addition, PilT4 was required to reduce iron oxides. Taken together, the results indicate that PilT4 is the motor ATPase of G. sulfurreducens pili and reveal a previously unrecognized role for pilus retraction in extracellular electron transfer, a strategy that confers on Geobacter spp. an adaptive advantage for metal reduction in the natural environment.
Highlights
The hallmark of the physiology of bacteria in the family Geobacteraceae is their ability to conserve energy for growth by transferring respiratory electrons to extracellular Fe(III) oxide minerals, a process that requires the expression of conductive type IV pili (T4P) (Reguera et al, 2005)
The genome of G. sulfurreducens contains four genes annotated as pilT that code for proteins containing the four conserved signature sequences (Walker A and B motifs and Asp and His boxes) of the secretion ATPase protein superfamily that PilT retraction ATPases belong to Savvides (2007)
All of the PilT paralogs encoded in the genome of G. sulfurreducens contain a Walker A motif with a conserved lysine for ATPbinding, a Walker B motif with a conserved glutamate residue for Mg2+-binding and ATP hydrolysis, and Asp and His boxes with conserved aspartic and histidine residues, respectively, which are essential for PilT activity (Figure 1; Walker et al, 1982; Savvides, 2007; Chiang et al, 2008; Jakovljevic et al, 2008)
Summary
The hallmark of the physiology of bacteria in the family Geobacteraceae is their ability to conserve energy for growth by transferring respiratory electrons to extracellular Fe(III) oxide minerals, a process that requires the expression of conductive type IV pili (T4P) (Reguera et al, 2005). Geobacter T4P are homopolymers of a single pilin subunit (PilA) (Cologgi et al, 2011), a short peptide (61 amino acids in the model representative Geobacter sulfurreducens) that retains the conserved amino-terminal features of type IVa pilins but diverges in amino acid composition and structure at the carboxy-terminus (Feliciano et al, 2012). This places the Geobacter pilins in an independent line of descent among bacterial type IV pilins and pseudopilins (Reguera et al, 2005).
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